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NEED INTRO SENTENCE TO HOOK READERS. The symbiosis between coral and their single-celled dinoflagellate symbionts, Symbiodinium, is the foundation of reef ecosystems, and a critical element of reef resilience [16; Muller-Parker2015-sd]. The coral holobiont responds to environmental conditions, and is the unit that interacts with the broader reef community17, supporting reef diversity and function across taxa (or at a global scale?). There is much genetic, functional, and response diversity within the Symbiodinium genus. Although Symbiodinium is currently classified as a single genus, it contains diversity similar to diversity found within other dinoflagellate orders6, and is divided into nine clades and hundreds of types18–20. There is much debate about species classifications within Symbiodinium, which has hampered species naming within Symbiodinium [21; but see 22) although Symbiodinium types are generally considered putative species [23. Symbiodinium types have distinct geographic distributions, host associations, and environmental optima24. Furthermore, total and relative abundance of Symbiodinium can vary among coral colonies, across environmental gradients, and over time25, with increased Symbiodinium abundance leading to increased environmental sensitivity and bleaching risk26. There are functional differences between Symbiodinium clades27, and Symbiodinium associations can range from mutualistic to neutral to parasitic based on Symbiodinium type as well as environmental conditions11. Recent advances in next-generation sequencing techniques have revealed cryptic genetic diversity within symbiotic Symbiodinium28–30, and has allowed for long-term genetic and ecological comparisons of symbiont community structure31.
Corals exhibit varying levels of symbiotic flexibility, but this flexibility comes with functional tradeoffs. Corals that host flexible symbioses (generalists) may be more sensitive to environmental perturbations than those with intimate symbioses (specialists)32. The adaptive bleaching hypothesis suggests that corals bleach in order to expel environmentally sub-optimal symbionts, followed by switching (picking up new symbionts from the environment) or shuffling (an internal change in dominant symbiont type or overall symbiont community structure)7,33–35. There is ample evidence for Symbiodinium shuffling (Rowan 2004), and a recent study showed evidence for Symbiodinium switching36. However, what remains unclear is if and how frequently bleaching events can actually be considered adaptive. Changes in photosynthetic efficiency during bleaching as well as bleaching resistance have been shown to correspond to distinct Symbiodinium phylotypes37. Clade D Symbiodinium are proported to have an enhanced thermal tolerance38, and repopulation of a coral host with clade D symbionts after a bleaching event is proposed to be a survival mechanism39–41. A history of thermal stress increased the prevalence of clade D Symbiodinium in a generalist coral species, but did not instigate similar changes in two specialist coral species42. Although the prevalence of clade D Symbiodinium increases during thermal stress and may increase thermal tolerance39, corals that house clade D symbionts may have slower growth rates8 or lower energy storage43. Furthermore, functional differences exist not only at the clade level, but are present among types within a single clade44.
The current paradigm of coral bleaching and recovery states that the stress must cease for coral to regain their symbiosis. Coral bleaching is the loss of obligate symbionts (Symbiodinium) from the coral tissue13,45. Thermal stress is the primary cause for coral bleaching, and can cause not only the breakdown of coral symbioses, but also cause coral mortality [46; CITE]. Thermal stress can be exacerbated by other environmental stressors (Cooper et al 2011, Béraud et al 2013, Maina et al 2008), and in turn, exacerbates ocean acidification (Gibbin et al 2015). The current paradigm of coral bleaching and resilience is that as environmental stress (such as warming) increases, corals begin to bleach. Extreme or long-lasting warming causes a complete breakdown of the coral symbioses, leading to expulsion of all (or nearly all) Symbiodinium from the coral host tissue. It has been shown that during bleaching, there is a window for recovery, that is, a certain amount of time during which the warming must cease and conditions must return to normal so that the coral can regain its symbionts. If the window for recovery passes without amelioration of the environmental conditions, the coral will starve and die. (Cunning et al 2016, Putnam et al 2017). Here we show that despite unprecedented heat stress, some corals exhibited resilience and survived. Survival through such an extreme heat event provides an exceptional opportunity to understand how some corals can withstand intense heat stress, and how corals in general might survive long-term warming. Remarkably, we find that some coral colonies were able to survive this prolonged heat stress by regaining their symbionts while temperatures were still elevated.
Global coral bleaching is increasing, and the 2014-2017 event caused a catastrophic loss of corals around the globe. There was up to 95% mortality in some regions during the 1997/1998 El Niño event (Glynn 1993). The 2014-2017 global coral bleaching event caused coral bleaching across the world’s oceans (Eakin 2016, Normile 2016), with up to 75% bleaching on some reefs in Hawaii, and at least some level of bleaching across 93% of the Great Barrier Reef (Minton et al 2015, GBRMPA 2016). The 2015-2016 El Niño, superimposed on nearly-ubiquitous tropical ocean warming, instigated the third global coral bleaching event (???). Our study location, Kiritimati Atoll (Christmas Island, Kiribati, Central Equatorial Pacific, Coordinates: 2, -157.4), was at the epicenter of this extreme El Niño event. Thermal anomalies were severe on Kiritimati, rapidly exceeding NOAA Coral Reef Watch’s Coral Bleaching Alert Level 1 (4 Degree Heating Weeks, DHW, a metric of cumulative thermal stress) and Alert Level 2 (8 DHW) thresholds, reaching an unprecedented (47) 25.7 DHW over a year-long bleaching event, demolishing most of the reef (???). Despite these staggering losses, some corals have the capacity to be resilient to these increasingly frequent mass-bleaching events (Hughes et al 2017). Here, we assess coral symbiosis and survival during the massive 2015/2016 El Niño event. We tagged, sampled, and photographed the same coral colonies before, during, and immediately after the El Niño event. We assessed bleaching condition and survival for each coral colony, and used Illumina MiSeq ITS2 amplicon sequencing and 97% de novo OTU clustering to evaluate changes in Symbiodinium community structure. To investigate mechanisms underlying the ability of these corals to not only survive a year of continuous heat stress, but to recover in the interim, we assessed the relationship between human disturbance, pre-bleaching Symbiodinium community structure, and coral survival, as well as the timing of Symbiodinium community shifts throughout this El Niño event. We document, for the first time, corals that were able to visually recover from bleaching, and to regain their Symbiodinium communities during the course of an extreme heat stress event. These corals (family Faviidae; Platygyra sp. and Favites sp.) were bleached within two months of the onset of warming, but had visibly recovered after 10 consecutive months of intense warming (Fig. 1).
